Limits...
From limbs to leaves: common themes in evolutionary diversification of organ form.

Mentink RA, Tsiantis M - Front Genet (2015)

Bottom Line: Second, species-specific expression of the newly discovered REDUCED COMPLEXITY homeodomain transcription factor influences growth between individual outgrowths after their initiation.These findings demonstrate that in both plants and animals tinkering with either patterning or post-patterning processes can cause morphological change.They also highlight the considerable flexibility of morphological evolution and indicate that it may be possible to derive broad principles that capture how morphogenesis evolved across complex eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research , Cologne, Germany.

ABSTRACT
An open problem in biology is to derive general principles that capture how morphogenesis evolved to generate diverse forms in different organisms. Here we discuss recent work investigating the morphogenetic basis for digit loss in vertebrate limbs and variation in form of marginal outgrowths of angiosperm (flowering plant) leaves. Two pathways underlie digit loss in vertebrate limbs. First, alterations to digit patterning arise through modification of expression of the Patched 1 receptor, which senses the Sonic Hedgehog morphogen and limits its mobility in the limb bud. Second, evolutionary changes to the degree of programmed cell death between digits influence their development after their initiation. Similarly, evolutionary modification of leaf margin outgrowths occurs via two broad pathways. First, species-specific transcription factor expression modulates outgrowth patterning dependent on regulated transport of the hormone auxin. Second, species-specific expression of the newly discovered REDUCED COMPLEXITY homeodomain transcription factor influences growth between individual outgrowths after their initiation. These findings demonstrate that in both plants and animals tinkering with either patterning or post-patterning processes can cause morphological change. They also highlight the considerable flexibility of morphological evolution and indicate that it may be possible to derive broad principles that capture how morphogenesis evolved across complex eukaryotes.

No MeSH data available.


Related in: MedlinePlus

Diversification of both patterning and post-patterning processes contributed to morphological variation of leaves and limbs. (A) In the vertebrate limb bud Fgf8 (green) expression from the apical ectodermal ridge (AER) stimulates proximodistal outgrowth, while posteriorly expressed Ptch1 (blue), through sequestration, creates a posterior to anterior SHH gradient that patterns the individual digits. In later stages, Fgf8 is maintained only in the AER, overlying digits that will completely form, while Msx2 (orange) expression is turned on in the interdigital tissue, triggering apoptosis. In the 3-toed jerboa and camel, expanded Msx2 expression causes the regression of the outermost digits (indicated by arrowheads). In the pig, Ptch1 expression is reduced to eliminate digit I (indicated by a star), a change that is not observed in the closely related camel. Ant, anterior; Post, posterior; P, proximal; D, distal. (B) Simple and dissected leaves similarly initiate as small leaf primordia (LP) from the shoot apical meristem (SAM) at sites where auxin maxima (yellow) are defined by CUC (purple) and PIN1 expression, but only dissected leaves reactivate KNOX (red) expression to suppress leaf cell differentiation. This allows the initial marginal outgrowths, patterned by CUC and PIN1, to develop into leaflets instead of serrations. Species-specific local expression of RCO (blue-green) in Cardamine hirsuta restricts cellular growth within leaf sinuses, thereby allowing separation of individual leaflets through modulation of local growth rates. P, proximal; D, distal.
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Figure 1: Diversification of both patterning and post-patterning processes contributed to morphological variation of leaves and limbs. (A) In the vertebrate limb bud Fgf8 (green) expression from the apical ectodermal ridge (AER) stimulates proximodistal outgrowth, while posteriorly expressed Ptch1 (blue), through sequestration, creates a posterior to anterior SHH gradient that patterns the individual digits. In later stages, Fgf8 is maintained only in the AER, overlying digits that will completely form, while Msx2 (orange) expression is turned on in the interdigital tissue, triggering apoptosis. In the 3-toed jerboa and camel, expanded Msx2 expression causes the regression of the outermost digits (indicated by arrowheads). In the pig, Ptch1 expression is reduced to eliminate digit I (indicated by a star), a change that is not observed in the closely related camel. Ant, anterior; Post, posterior; P, proximal; D, distal. (B) Simple and dissected leaves similarly initiate as small leaf primordia (LP) from the shoot apical meristem (SAM) at sites where auxin maxima (yellow) are defined by CUC (purple) and PIN1 expression, but only dissected leaves reactivate KNOX (red) expression to suppress leaf cell differentiation. This allows the initial marginal outgrowths, patterned by CUC and PIN1, to develop into leaflets instead of serrations. Species-specific local expression of RCO (blue-green) in Cardamine hirsuta restricts cellular growth within leaf sinuses, thereby allowing separation of individual leaflets through modulation of local growth rates. P, proximal; D, distal.

Mentions: Cooper et al. (2014) studied the evolutionary changes that resulted in convergent digit loss in different mammalian species. A mammalian limb (such as a leg) is attached to the body at one (proximal) end and has 1 to 5 anteroposteriorly distinct digits (e.g., toes) at the other (distal) end. Limbs develop from the limb bud through the sequential action of several distinct signaling centers (Figure 1A; Butterfield et al., 2010). Bone morphogenetic proteins (BMPs) specify the formation of the apical ectodermal ridge (AER) at the distal end of the limb bud, from which fibroblast growth factors (FGFs) are secreted to stimulate proximodistal outgrowth (Lewandoski et al., 2000; Pizette et al., 2001; Boulet et al., 2004). The morphogen Sonic hedgehog (SHH) is secreted from the posterior limb bud to direct both digit patterning and expansion of the hand- or footplate to accommodate all digits (Harfe et al., 2004; Towers et al., 2008). Subsequent digit elongation is controlled by FGFs secreted from the AER and in later stages BMPs sculpt the limb by inducing apoptotic cell death within interdigital tissue in concert with the transcription factor Msx2 (Marazzi et al., 1997; Ferrari et al., 1998; Sanz-Ezquerro and Tickle, 2003).


From limbs to leaves: common themes in evolutionary diversification of organ form.

Mentink RA, Tsiantis M - Front Genet (2015)

Diversification of both patterning and post-patterning processes contributed to morphological variation of leaves and limbs. (A) In the vertebrate limb bud Fgf8 (green) expression from the apical ectodermal ridge (AER) stimulates proximodistal outgrowth, while posteriorly expressed Ptch1 (blue), through sequestration, creates a posterior to anterior SHH gradient that patterns the individual digits. In later stages, Fgf8 is maintained only in the AER, overlying digits that will completely form, while Msx2 (orange) expression is turned on in the interdigital tissue, triggering apoptosis. In the 3-toed jerboa and camel, expanded Msx2 expression causes the regression of the outermost digits (indicated by arrowheads). In the pig, Ptch1 expression is reduced to eliminate digit I (indicated by a star), a change that is not observed in the closely related camel. Ant, anterior; Post, posterior; P, proximal; D, distal. (B) Simple and dissected leaves similarly initiate as small leaf primordia (LP) from the shoot apical meristem (SAM) at sites where auxin maxima (yellow) are defined by CUC (purple) and PIN1 expression, but only dissected leaves reactivate KNOX (red) expression to suppress leaf cell differentiation. This allows the initial marginal outgrowths, patterned by CUC and PIN1, to develop into leaflets instead of serrations. Species-specific local expression of RCO (blue-green) in Cardamine hirsuta restricts cellular growth within leaf sinuses, thereby allowing separation of individual leaflets through modulation of local growth rates. P, proximal; D, distal.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4561821&req=5

Figure 1: Diversification of both patterning and post-patterning processes contributed to morphological variation of leaves and limbs. (A) In the vertebrate limb bud Fgf8 (green) expression from the apical ectodermal ridge (AER) stimulates proximodistal outgrowth, while posteriorly expressed Ptch1 (blue), through sequestration, creates a posterior to anterior SHH gradient that patterns the individual digits. In later stages, Fgf8 is maintained only in the AER, overlying digits that will completely form, while Msx2 (orange) expression is turned on in the interdigital tissue, triggering apoptosis. In the 3-toed jerboa and camel, expanded Msx2 expression causes the regression of the outermost digits (indicated by arrowheads). In the pig, Ptch1 expression is reduced to eliminate digit I (indicated by a star), a change that is not observed in the closely related camel. Ant, anterior; Post, posterior; P, proximal; D, distal. (B) Simple and dissected leaves similarly initiate as small leaf primordia (LP) from the shoot apical meristem (SAM) at sites where auxin maxima (yellow) are defined by CUC (purple) and PIN1 expression, but only dissected leaves reactivate KNOX (red) expression to suppress leaf cell differentiation. This allows the initial marginal outgrowths, patterned by CUC and PIN1, to develop into leaflets instead of serrations. Species-specific local expression of RCO (blue-green) in Cardamine hirsuta restricts cellular growth within leaf sinuses, thereby allowing separation of individual leaflets through modulation of local growth rates. P, proximal; D, distal.
Mentions: Cooper et al. (2014) studied the evolutionary changes that resulted in convergent digit loss in different mammalian species. A mammalian limb (such as a leg) is attached to the body at one (proximal) end and has 1 to 5 anteroposteriorly distinct digits (e.g., toes) at the other (distal) end. Limbs develop from the limb bud through the sequential action of several distinct signaling centers (Figure 1A; Butterfield et al., 2010). Bone morphogenetic proteins (BMPs) specify the formation of the apical ectodermal ridge (AER) at the distal end of the limb bud, from which fibroblast growth factors (FGFs) are secreted to stimulate proximodistal outgrowth (Lewandoski et al., 2000; Pizette et al., 2001; Boulet et al., 2004). The morphogen Sonic hedgehog (SHH) is secreted from the posterior limb bud to direct both digit patterning and expansion of the hand- or footplate to accommodate all digits (Harfe et al., 2004; Towers et al., 2008). Subsequent digit elongation is controlled by FGFs secreted from the AER and in later stages BMPs sculpt the limb by inducing apoptotic cell death within interdigital tissue in concert with the transcription factor Msx2 (Marazzi et al., 1997; Ferrari et al., 1998; Sanz-Ezquerro and Tickle, 2003).

Bottom Line: Second, species-specific expression of the newly discovered REDUCED COMPLEXITY homeodomain transcription factor influences growth between individual outgrowths after their initiation.These findings demonstrate that in both plants and animals tinkering with either patterning or post-patterning processes can cause morphological change.They also highlight the considerable flexibility of morphological evolution and indicate that it may be possible to derive broad principles that capture how morphogenesis evolved across complex eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research , Cologne, Germany.

ABSTRACT
An open problem in biology is to derive general principles that capture how morphogenesis evolved to generate diverse forms in different organisms. Here we discuss recent work investigating the morphogenetic basis for digit loss in vertebrate limbs and variation in form of marginal outgrowths of angiosperm (flowering plant) leaves. Two pathways underlie digit loss in vertebrate limbs. First, alterations to digit patterning arise through modification of expression of the Patched 1 receptor, which senses the Sonic Hedgehog morphogen and limits its mobility in the limb bud. Second, evolutionary changes to the degree of programmed cell death between digits influence their development after their initiation. Similarly, evolutionary modification of leaf margin outgrowths occurs via two broad pathways. First, species-specific transcription factor expression modulates outgrowth patterning dependent on regulated transport of the hormone auxin. Second, species-specific expression of the newly discovered REDUCED COMPLEXITY homeodomain transcription factor influences growth between individual outgrowths after their initiation. These findings demonstrate that in both plants and animals tinkering with either patterning or post-patterning processes can cause morphological change. They also highlight the considerable flexibility of morphological evolution and indicate that it may be possible to derive broad principles that capture how morphogenesis evolved across complex eukaryotes.

No MeSH data available.


Related in: MedlinePlus